Diversity of life cycles, breeding systems, and mating types in mushrooms

Mushrooms beneficial for human nutrition and health mainly belong to the phyla Ascomycota, subphylum Pezizomycotina, or Basidiomycota, subphylum Agaricomycotina. Mushrooms are large fruiting bodies habitually produced for sexual reproduction via meiotic spores, either ascospores or basidiospores. Most mushroom species are heterothallic, requiring two self-sterile homokaryotic organisms with distinct haploid nuclei to mate and form a fertile heterokaryotic cell stage with two types of haploid nuclei capable of developing into the fruiting bodies and undergoing karyogamy, meiosis and sexual sporulation in specialized cells (meiosporangia). Mating, and possibly subsequent steps in fruiting body formation, are genetically controlled by different information localized at the mating-type loci in the haploid nuclei of mating-compatible partners. Few species or special self-fertile homokaryotic isolates within some species are homothallic and can reproduce without compulsory mating with another strain. Homothallic reproduction leads to inbreeding, in contrast to the outcrossing favored by heterothallism. Inbreeding can also be caused by rare mechanisms of pseudo-homothallism in which two haploid nuclei of different mating types are included in a single heterokaryotic meiospore. Germination of spores of pseudo-homothallic species leads directly to fertile heterokaryotic mycelia. This article describes life cycles of selected hetero-thallic model asco- and basidiomycetes and explains genetic structures and functions of their mating-type (mat) loci. Ascomycetes have a single locus (MAT1) with two idiomorphs that alternatively encode unrelated MATα1 HMG-box or HMG-box transcription factors (TFs) as key developmental regulators. Additional genes may be present in either idiomorph, depending on the taxon. Most basidiomycetes are heterothallic tetrapolar with two unlinked multigenic mat loci, whose different alleles determine their multiple mating-type specificities. matHD encodes two types of homeodomain TFs (HD1 and HD2), and matPR encodes pheromones and pheromone receptors. matHD is the only segregating mat locus in bipolar basidiomycete species. Information is given on breeding systems and life cycles of important commercial heterothallic and homothallic mushroom species and genetic changes from hetero- to homothallism are discussed.